As Nico Rosberg topped first free practice ahead of Lewis Hamilton, Verstappen managed 21 laps of the Suzuka circuit before having to pull over as smoke gushed from his car.
"I have a problem in the engine, it's not pulling any more," the Dutchman, who will replace Jean-Eric Vergne next season, radioed to his team as he hit trouble. "I have smoke out of the engine. What should I do?"
It was a rude introduction to Formula One for the Dutch 17-year-old, who is the son of ex-F1 driver Jos and whose entry in the sport has sparked much debate.
Spain's two-times world champion Fernando Alonso was third quickest for Ferrari and the only driver to come within a second of the two Mercedes with Finn Valtteri Bottas fourth for Williams, ahead of countryman Kimi Raikkonen in the second Ferrari.
Danish driver Kevin Magnussen was sixth in his McLaren, two places quicker than teammate Jenson Button of Britain.
Australian Daniel Ricciardo again outperformed Red Bull partner and four-time defending world champions champion Sebastian Vettel, by posting the seventh quickest lap.
Russian Daniil Kvyat rounded out the top 10 in the first of the Toro Rosso cars, two places ahead of his temporary team-mate Verstappen.
The sun came out for the first free practice but race organisers are anxiously monitoring the progress of a typhoon gathering intensity off the Japanese mainland.
